We report on the pioneering discovery of Devonian fish remains in the Paraná Basin, which represents the southernmost record of fishes from that period in mainland South America. The material comes from an outcrop at the lower portion of the São Domingos Formation, within Sequence C of the Paraná-Apucarana sub-basin in Tibagi, State of Paraná. Marine invertebrates are abundant in the same strata. The dark colored fish remains were collected in situ and represent natural moulds of partially articulated shark fin rays (radials). No elements such as teeth or prismatic cartilage have been preserved with the fins rays. This can be attributed to the dissolution of calcium-phosphatic minerals at the early stages of fossilization due to diagenetic processes possibly linked to strong negative taphonomic bias. This may have contributed to the fact that fishes remained elusive in the Devonian strata of this basin, despite substantial geological work done in the Paraná State in recent decades. In addition, the scarcity of fish fossils may be explained by the fact that the Devonian rock deposits in this basin originated in a vertebrate impoverished, cold marine environment of the Malvinokaffric Realm, as previously suspected.

The Devonian was a pivotal time for the evolution of fishes and one in which all the large classes of fishes co-existed. Many of the groups that dominated the seas and continental waters at the time did not survive the end of the Devonian. Notably, placoderms and acanthodians whose remains are relatively abundant in South America are among the groups that are confined to the Palaeozoic.

The fossil material was collected at an outcrop in the vicinity of the km 220 of highway BR 153 in the municipality of Tibagi, Paraná State in southern Brazil (24°38’2,19”S 50°27’40,35”O and UTM22J 54533,28mE 7275485,35mS) (Figure 1). The specimens are deposited in the Laboratory of Stratigraphy and Palaeontology of the State University of Ponta Grossa (UEPG, Ponta Grossa, state of Paraná, southern Brazil).

Figure 1 Location map of the fossiliferous outcrop (1) in the State of Paraná, Brazil.

Two of the specimens (UEPG/DEGEO MPI 9959 and UEPG/DEGEO MPI 10548) have been micro-CT scanned in Rio de Janeiro, but no additional anatomical information was accessible from the scans, nor further fish material was found inside the rock matrix.

The fieldwork was undertaken over the last ten years along the main section Tibagi-Telêmaco Borba originally described by Bergamaschi (1999), and Tibagi-Alto do Amparo section (Bosetti and Horodyski 2008) as well as at localities comprising the boundary between the Ponta Grossa and São Domingos formations, including the Tibagi Member sensu Oliveira (1912) and Grahn et al. (2013). The fossil material was collected utilizing the taphonomic method described by Ghilardi and Simões (2000) and the taphofacies analyses done observing the criteria established by Speyer and Brett (1986, 1988). The taphonomic methodology consisted in the identification of the skeletal types present in the associations (bivalve, univalve, multi-element) and taphonomic signatures (shelly packing, size selection, fragmentation and disarticulation degree, and bioclast orientation in relation to the bedding plane). Signatures such as abrasion, corrosion and rounding have not been detected in any bioclasts; however, the presence/absence of those signatures was utilized to interpret the different hydrodynamic/energy regimes present in the basin. We also recorded lithological and sedimentary structures associated with the fossils, based on the interpretations provided by Walker and Plint (1992). We have adapted these methodologies to the situation observed in the Devonian rocks of the Paraná basin. Storm deposits interpretation followed Miller et al. (1988).

GEOLOGICAL SETTING

The Paraná Basin is a large intracratonic basin (about 1,700,000 km2) located in southernmost Brazil and north/northwestern Uruguay, parts of Paraguay and Argentina (Figure 2a). The basin is approximately 1,750 km long and 900 km wide, predominantly along a NE-SW axis. The sedimentary fill of the basin was influenced by tectonic-eustatic cycles linked to the evolution of Western Gondwana during the Paleozoic and Mesozoic (Milani and Ramos 1998, Milani et al. 2007).

Figure 2 a. Location map of the study area in the Paraná Basin record. b. Stratigraphic position of the interval analyzed herein (= rectangle) within the Paraná Supersequence (modified of the Milani and Ramos 1998, Milani et al. 2007).

The basin developed over distinct geotectonic domains, comprising Archean and Early Proterozoic cratonic terranes and Late Proterozoic mobile belts related to the Pan-african and Brazilian cycles that were responsible for the assemblage of Western Gondwana. Hence, the geotectonic framework of the basement is characterized by several cratonic blocks and intervening mobile belts, forming a complex framework of lineaments and crustal discontinuities that influenced sedimentation patterns due to differential subsidence and uplift of the tectonic blocks (Holz et al. 2006).

Eustatic-tectonic cycles controlled the sedimentation rates in the Paraná Basin and generated a stratigraphic record that is marked by numerous subaqueous events that produced erosion as well as non-deposition surfaces. Milani and Ramos (1998) and Milani et al. (2007) described six, second order depositional sequences for this basin, ranging in age from Late Ordovician to Late Cretaceous. The stratigraphic interval studied here corresponds to the second sequence of Milani et al. (2007), namely the “Paraná Supersequence,” ranging from probably the latest Silurian (Pridolian) to Devonian (Figure 2b). It is a succession lithostratigraphycally divided into three formations: Furnas, Ponta Grossa and São Domingos (Grahn et al. 2013). The new stratigraphic and paleontologic data described here was acquired from an outcrop represented by a section located in Tibagi County, Paraná State (Figure 3).

Figure 3 Chronostratigraphic scheme for the Early Devonian interval in the Paraná Basin, Brazil (modified from Grahn et al. 2013). The arrow indicates the provenance of the shark fin remains described here.

The investigated outcrop belongs to the São Domingos Formation (Grahn 1992, Grahn et al. 2000, 2013, Mendlowicz Mauller et al. 2009), and span from the late Emsian age (Figure 3). A stratigraphic profile (Figure 4) was drawn along the Tibagi-Alto do Amparo section (Bosetti and Horodyski 2008, Horodyski 2014; see also Figure 1). The outcrops were stratigraphically stacked and correlated with the sequence framework of Bergamaschi (1999), Bergamaschi and Pereira (2001), which was updated by Grahn et al. (2013). The Devonian of the Apucarana Sub-basin was divided into six 3rd. order depositional sequences by the authors mentioned above. These sequences are numbered A-F. The studied outcrop is located within the transgressive system tract (TST) of the base of Sequence C of Horodyski (2014). According to Bergamaschi and Pereira (2001), the TST of Sequence C is characterized by a retrogradational facies trend, grading from fine-grained sandstones and siltstones to dark mudstones representing the maximum transgressive surface. At the topmost portion of this sequence, the progradational patterns of the facies succession are taken as an indicative of a highstand systems tract, recording the normal regression that followed the transgressive phase.

Figure 4 Composite stratigraphic column based on a series of profiles drawn along the Tibagi-Ventania section (see Figure 1) indicating the provenance of the chondrichthyan fin remains (lithostratigraphy based on Bosetti and Horodyski (2008) and Horodyski (2014). TST = Transgressive system tract; HCS = Hummocky cross-stratification.

FACIES

Conglomerate and coarse to fine sandstones, siltstones and shales dominate the Lower and Middle Devonian rocks in the studied region. Neither palynofacies nor geochemical studies were undertaken to date; therefore, the facies analysis is only based either on contemporaneous or post-depositional composition, color, texture, and structure. Only the fossil-bearing facies necessary for the taphofacies analysis will be described.

The facies SL-hcs (fine sandstones to coarse siltstones with thin interspersing sand lenses) represents the more distal shoreface zone, above the FWWB. The chondrichthyan fin remains were found in this facies.

The facies SL (massive siltstones) represents the distal shoreface to offshore transition. SL-p (siltstones often interspersed with thin sand lenses) indicates the offshore transitional zone below the lower shoreface. This region is located between the FWWB and the storm wave base level (SWB), marking the transition with the offshore, and is influenced by storm flows, represented by the thin, centimeter-scale, sand lenses locally recorded. Facies SH-f and SH-l, are interpreted as the deepest, offshore deposits with stagnant muds (SH-f) and dark shales (SH-l) formed by fine sediment decantation, after storm flows. This facies is found below the SWB.

Taphonomic attributes: Dense pavements of entire and articulated shells, associate with a few disarticulated elements. Fragmentation, corrosion, abrasion and bioerosion are absent. Echinasterella is also abundant and complete. Fossils are oriented parallel to the bedding plane. All fossils are poorly packing throughout the matrix with no hydrodynamics preferential orientation. The chondrichthyan vertebrates are disarticulated, with only complete fins are registered, and no predation record.

Interpretation and discussion (Lower shoreface storm-dominated): this taphofacies marks the lower shoreface region of the basin, above the FWWB. Fair-weather waves sporadically affected sedimentation, but no hydrodynamic selection was observed. Disarticulated brachiopods and chondrichthyan fin remains indicate post-mortem disarticulation due to bottom-level hydraulic processes and/or necrolysis at short residence time. Furthermore, the occurrence of articulated Australospirifer, complete Echinasterella and chondrichthyan fin remains associated with HCS, indicates increase in the sedimentation rates (very high) with large masses of sediment deposited in a short-lived event, burying in situ some fauna (Echinasterella and articulated Australospirifer). Spatial and temporal mixing (Kidwell and Bosence 1991) is moderate to high in this taphofacies, generating accumulations of bioclasts of different sizes. Consequently, the high sedimentation rate deposited the remains promptly below the taphonomically active zone (inert zone) and enhanced their preservation (Davies et al. 1989, Olszewski 1999, 2004). This was possible due to the retrogradational stacking and accommodation space of the TST in the 3rd order Devonian sequence C of the Paraná Basin.

According to Elder and Smith (1988), partial articulation of fish remains (e.g. only fins) taphonomically indicates undecayed connective tissue. Experiments developed by Smith and Elder (1985), following Schaefer (1972), show that the partial disarticulation of skeletons such as observed by Zangerl and Richardson (1963) can be the result of bacterial decay and flotation in warm waters (Elder and Smith 1988). However, during Devonian times the Malvinokaffric fauna inhabited cold, shallow marine seas at paleolatitudes ranging between 60°- 80° S, according to Torsvik and Cocks (2013) and Melo (1988). The curious and apparently inexplicable absence of fossil fishes (prior to our recent discovery) in the Apucarana Sub-basin may be explained by selective damage caused by biostratinomic and diagenetic factors. In this particular assemblage, apparently a rapid deposition of fish carcases within a taphonomically inert zone has occurred. The quick burial prevented total decay of the cartilaginous skeletal elements (c.f. Elder and Smith 1988), but these have mostly been preserved as impressions and molds of the original material.

Material: The three specimens, UEPG/DEGEO MPI 9959 E UEPG/DEGEO MPI 105481 and UEPG/DEGEO MPI 10709 come from an outcrop located in the vicinity of Km 220 of the BR 153 highway and were collected within a 30 cm thick stratum. All the samples have been collected in situ in rocks of the São Domingos Formation, Sequence C of Bergamaschi and date from early Late Emsian.

Description:

UEPG/DEGEO/MPI 9959 (Fig. 5a, b, c). The specimen represents partially articulated remains of a fin, preserved as very dark colored impressions (natural casts) of proximal and distal, rod-shaped radial elements. This specimen is 31.6 mm long and 0.83 mm wide, but the actual size of the complete fin is unknown. The preserved part of this fin shows clear radials zonation: The proximal ones, eleven of which are preserved, are mostly unsegmented and at least twice as broad as the distal ones, which are all segmented and show extensive branching. The girdle cartilages have not been preserved.

UEPG/DEGEO/MPI 10709 (Fig. 6a, b): Partially articulated, but largely in disarray remains of a fin showing only impressions (natural casts) of some 60 rod-shaped radial elements. The preserved parts of this very distorted specimen measure approximately 36 x 16 mm.

The chondrichthyan material from the Paraná Basin described here is too poorly preserved as to permit its attribution to any described taxa. Previously, disarticulated chondrichthyan remains were reported from the Parnaíba and the Amazon basin in Brazil as well as from other Devonian rocks elsewhere in South America. These include teeth, finspines, cartilage fragments in concretions and a braincase (Maisey 2001, Janvier and Maisey 2010). However, none of fossils described so far can be directly compared to these fin impressions found in the Devonian Paraná Basin. The only other fin remains known from South America come from Bolivia and have been attributed to the genus Zamponiopteron (Anderson et al.1999a), which apparently lacked any cartilage calcifications. According to Janvier and Maisey (2010), the closely set fin radials of the chondrichthyan Pucapampella from South Africa (a genus also occurring in the Belen Formation of Bolivia) resembles Zamponiopteron Janvier and Suárez-Riglos 1986. The systematic position of Zamponiopteron remains uncertain. Only known from ‘fin plates’ fossilized inside concretions which are relatively abundant in the Devonian of Bolivia, its fin radials are strangely ankilosed to the triangular plate, which make the fins resemble the ‘zampoñas’ or Bolivian flutes (see Janvier 2003). The radials of Zamponiopteron possess numerous longitudinal vascular grooves (Janvier 2003, fig. 4), which in our opinion preclude them from matching the anatomy of any known chondrichthyan radials and favoring a placoderm affinity instead. The ‘flute-like’ proximal part of the radials inside the fin plate suggests that they could articulate with placoderm basals (e.g. Carr et al. 2010, fig. 3).

The Brazilian fin remains from the Paraná Basin differ on all accounts from Zamponiopteron. None of three specimens described here show any signs of being attached to a mineralized fin plate.

Both pectoral and pelvic fins of chondrichthyans possess long, segmented radials (e.g. Coates 2003, fig. 4). The non-preservation of basal elements hinders the identification of the anatomical positions of these three fin remains.

COULD THE BRAZILIAN FIN RAYS BELONG TO PLACODERMS?

The radial elements of placoderm fins are rarely preserved and are very poorly known. Carr et al. (2010) undertook a revision of basal and radial elements of the placoderm fins, pointing to the fact that radials are only known from two placoderm groups, namely DunkleosteusLehman 1956 and Gemundina stuertziGross 1963. Placoderm radials seem to differ from chondrichthyan radials and indeed from the material described here, by apparently being bony in nature (perichondral bone) and of equal size (Carr et al. 2010, fig. 4).

PREVIOUSLY KNOWN CHONDRICHTHYAN REMAINS FROM DE DEVONIAN OF BRAZIL

To date, chondrichthyans remains from the Devonian of Brazil have only been recorded from borehole cores and outcrops of the Amazon Basin and the Parnaíba Basin. The Early Lochkovian Manacapuru Formation of Pará has yielded isolated teeth, tooth whorls and fin spines (Janvier and Melo 1988, 1992), some of which may belong to chondrichthyans (Janvier and Maisey 2010).

The chondrichthyans Antarctilamna seriponensisGagnier (in Gagnier et al. 1988), occurs in the Late Lochkovian//Early Pragian of Seripona, Bolivia (Janvier and Maisey 2010); The Late Emsian/Early Eifelian localities of Bolivia have yielded placoderms and chondrichthyans, the latter comprising Pucapampella sp.,?Antarctilamnidae gen. et sp. indet. and also a gnathostome of uncertain affinities, namely Zamponiopteron triangularis Janvier and Suárez-Riglos 1986, Z. falciformis Janvier and Suárez-Riglos 1986 and Z. spirifera Janvier and Suárez-Riglos 1986. According to Janvier and Villarroel (2000), the chondrichthyan Antarctilamna occurs the Givetian of Australia, but is also found in rocks as old as Late Emsian in Iran and Saudi Arabia. The Bolivian records (Gagnier et al. 1988, 1989) possibly range from the Emsian up to the Frasnian.

DEVONIAN CHONDRICHTHYANS FROM VENEZUELA

Antactilamnid shark remains were reported from the Middle Devonian of Maturin Basin, Venezuela by Young et al. (2000).

Anderson et al. (1999b) provided an overview of the Devonian fish faunas of South Africa is provided by Emsian and Eifelian material is scarce and fragmentary and includes placoderm acanthodian and chondrichthyan remains. Diplodont teeth attributed to phoebodonts were reported, as well as teeth of Antarctilamna.

PALEOBIOGEOGRAPHIC SIGNIFICANCE AND TAPHONOMIC BIAS

Melo (1988) provided a comprehensive correlation of the Devonian rocks in South America and Africa as well as corresponding palaeogeographical reconstructions. His figures 4 an 5 (Melo 1988, pgs. 683-4) are of special interest as they correspond to the Emsian age. They show extensive marine connections between the Paraná Basin and western South America, but no connection with the Parnaíba and Amazon basins at the time.

Only disarticulated chondrichthyan remains have been recovered from the various Devonian fish bearing localities in South America to date. The apparent absence of an ichthyofauna of Devonian age in the Paraná Basin proved to be deceptive. The three recently discovered, partially articulated fish fins described herein provide the first evidence to suggest that sharks were indeed present in the ecosystems, although they were probably rare.

Taphonomic bias seems to have played an important role in the Devonian fossil record of the Paraná Basin. As the conditions in the Paraná Basin differ substantially from those in other Brazilian and South American basins. According to Sedorko et al. (2013), within the Paraná Basin, the interval Pridoli-Pragian is nearly devoid of body fossils. Invertebrates and ichnofossils are better known from the interval Neopraguian/Eo-Givetian. Although ichnofossils are abundant in both intervals, their stratigraphic distribution and taphonomy are still poorly known.

As previously pointed out by Maisey et al. (2002), ‘the best-known Malvinokaffric fishes are from the Emsian-Eifelian of Bolivia, including chondrichthyans (AntarctilamnaLong and Young 1995) Pucapampella, Zamponiopteron (for the latter, see Coates 2003), and placoderms (e.g., Bolivosteus apud Janvier and Suárez-Riglos 1986). Emsian Malvinokaffric vertebrates have also been described from South Africa, including forms similar or identical to Pucapampella and Zamponiopteron (Anderson et al.1999b). So far, Pucapampella, Zamponiopteron, and cf. Bolivosteus are known only from localities within the Malvinokaffric realm, suggesting that (like some of the invertebrates) they may be endemic Malvinokaffric taxa’ (Maisey et al. 2002, p. 709).

Spines of the acanthodian Machaeracanthus have been reported from several Malvinokaffric sites (mainly Emsian) in Brazil (Pimenteira formation, Parnaíba Basin; Campos 1964, Lelièvre et al.1993, Maisey et al. 2002), Antarctica (Young 1991, Webers et al.1992) and South Africa (Lower Bokkeveld Group; Anderson et al.1999a, b). This genus has been documented in the Amazon Basin (Katzer 1897), which contains “mixed” invertebrate assemblages including Malvinokaffric and Eastern Americas and European taxa, and is considered to be a biogeographic boundary area, with a postulated Emsian-Eifelian marine connection to Bolivia or southern Peru (Melo 1988, Maisey et al. 2002).

According to Maisey et al. (2002) the chondrichthyans Pucapampella and Zamponiopteron and the rhenanid placoderm Bolivosteus are known from the Andean and South African-Malvinan provinces, but they have not yet been reported from the Falklands or Antarctica, neither have they been found in anywhere in the Brazilian province. Machaeracanthus on the other hand, was not endemic to the Malvinokaffric realm, ‘its occurrence in several Malvinokaffric sites from Bolivia, the Falklands, South Africa and Antarctica makes it one of relatively few vertebrates known to have inhabited the cold, storm-dominate d circumpolar waters of that region, and it is the most widespread vertebrate known from this biogeographic realm’ (Maisey et al. 2002, p. 710).

CONCLUSIONS

The recent discovery of chondrichthyan fin remains in the Emsian of the Paraná Basin is very encouraging and further fish material is now expected to be found in rocks of the same region. The material collected to date is not sufficiently well preserved to allow for taxonomic identifications at generic and species level. Also, unfavorable diagenetic conditions seem to have prevailed in most if not all the Devonian strata of the Paraná basin, which led to dissolution of biogenic apatite and other biominerals leading vertebrates and invertebrates to fossilize mostly as impressions and molds.

ACKNOWLEDGMENTS

The authors thank Dr. Leonardo Borghi (UFRJ) and Dr. Alessandra Silveira Machado (UFRJ) for the micro-CT scan tests of two of the specimens. E.P. Bosetti thanks the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq/PQ 311483/2014-3) for financial support and the Plaios Group/UEPG for fieldwork; R.S. Horodyski thanks the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) the PNPD for research grant and Dr. John Maisey (American Museum of Natural History, USA) for early discussions.